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Intellectual disability and neurogenesis defects associated with increased turnover of an O-GlcNAcase variant

Authier, F.; Attianese, B.; Galan Bartual, S.; Mitchell, C. W.; Ferenbach, A. T.; Doummar, D.; Charles, P.; Mignot, C.; Keren, B.; van Aalten, D.

2023-11-24 neurology
10.1101/2023.11.23.23298195 medRxiv
Show abstract

Rare, high-impact genetic variants affecting genes essential for neurodevelopment represent a major contributing factor to uncharacterised intellectual disabilities. We present the first cases, population-based genetic evidence, an animal model and electrophysiological/functional dissection of pathogenic variants in OGA, a key regulator of protein O-GlcNAcylation, associated with cognitive and motor impairments. For a missense variant in the OGA C-terminal HAT domain, a dosage effect in genome-edited mouse embryonic stem cells is associated with impaired neuronal maturation. Mice harbouring this variant display altered brain OGA levels, while maintaining protein O-GlcNAcylation homeostasis. Hippocampal neurons exhibit altered developmental trajectories of neuronal network activity, mechanistically linked to pathways involved in synapse structure and function. We establish OGA variants as a cause of intellectual disability and show that partial reduction of OGA levels, even in the absence of global O-GlcNAc perturbation, impairs neuronal maturation and circuit function, highlighting a dosage-sensitive role for OGA in human neurodevelopment.

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